Efficacy and prognostic factors of second transurethral resection for non-muscle-invasive bladder cancer

AO Yangkun; LUO Weiming; RAN Qiang; WANG Haitao; ZHANG Jian; WANG Yapeng; WANG Ze; XU Jing; ZHANG Jun; CHEN Zhenzhen; LAN Weihua; LIU Qiuli; JIANG Jun

doi:10.16016/j.2097-0927.202506008

您当前的位置：

首页 >

文章列表页 >

Efficacy and prognostic factors of second transurethral resection for non-muscle-invasive bladder cancer

Clinical Medicine | 更新时间：2025-08-25

- Efficacy and prognostic factors of second transurethral resection for non-muscle-invasive bladder cancer
- Journal of Army Medical University Vol. 47, Issue 16, Pages: 1923-1930(2025)
- 作者机构：
  
  陆军特色医学中心（第三军医大学大坪医院）泌尿外科，重庆
- 作者简介：
  
  JIANG Jun， E-mail： Jun Jiang_64@163.com
- 基金信息：
  
  the General Program of National Natural Science Foundation of China(82172721);the Key Project of Natural Science Foundation of Chongqing(CSTB2024NSCQ-KJFZZDX0008);the Talent Innovation Capacity Training Plan of Army Medical Center of PLA(ZXZYTSLC04)
- DOI：10.16016/j.2097-0927.202506008
  CLC：
- Received：04 June 2025，
  
  Revised：13 July 2025，
  
  Published：30 August 2025
- 稿件说明：
移动端阅览
敖杨坤,罗伟铭,冉强,等.非肌层浸润性膀胱癌二次电切术后疗效评估及预后影响因素分析[J].陆军军医大学学报,2025,47(16):1923-1930.

AO Yangkun,LUO Weiming,RAN Qiang,et al.Efficacy and prognostic factors of second transurethral resection for non-muscle-invasive bladder cancer[J].J Army Med Univ,2025,47(16):1923-1930.
敖杨坤,罗伟铭,冉强,等.非肌层浸润性膀胱癌二次电切术后疗效评估及预后影响因素分析[J].陆军军医大学学报,2025,47(16):1923-1930. DOI：10.16016/j.2097-0927.202506008.

AO Yangkun,LUO Weiming,RAN Qiang,et al.Efficacy and prognostic factors of second transurethral resection for non-muscle-invasive bladder cancer[J].J Army Med Univ,2025,47(16):1923-1930. DOI：10.16016/j.2097-0927.202506008.

摘要

目的

探究非肌层浸润性膀胱癌（non-muscle-invasive bladder cancer，NMIBC）患者首次电切术后病灶残留的危险因素与二次电切术后肿瘤复发的危险因素，为临床诊疗提供参考。

方法

采用病例-对照研究设计方案，纳入2017年1月-2025年1月于陆军特色医学中心泌尿外科接受经尿道膀胱肿瘤切除术（transurethral resection of bladder tumors，TURBT）并于2~8周内再次行TURBT（二次电切）的120名NMIBC患者，根据首次TURBT术后是否存在病灶残留将患者分为病灶残留组34例、病灶未残留组86例，通过

检验和多因素Logistic回归分析可能影响TURBT后病灶残留的危险因素；通过单因素和多因素Cox回归模型分析可能影响二次电切术后肿瘤复发的危险因素。

结果

首次TURBT术后患者病灶残留率为28.33%，卡方检验分析发现肿瘤分期T1期（

=5.756，

=0.016）和肿瘤宽基底（χ

=4.331，

=0.037）是首次TURBT后病灶残留的影响因素，多因素Logistic回归结果显示肿瘤分期T1期（

=3.047，95%

：1.128~8.226，

=0.028）是首次TURBT后病灶残留的独立危险因素；二次电切术后患者肿瘤复发率为17.5%，多因素Cox回归结果显示肿瘤分期T1期［

=4.258，95%

：（1.248~14.532），

=0.021］、二次电切术后化疗药物灌注［

=3.539，95%

：（1.284~9.752），

=0.015］、泌尿系统肿瘤史［

=3.002，95%

：（1.145~7.873），

=0.025］、高PLR比值比［

=2.798，95%

：（1.115~7.023），

=0.028］是肿瘤复发的独立危险因素。

结论

首次TURBT术后肿瘤分期T1期、肿瘤宽基底是病灶残留的危险因素，二次电切术后肿瘤分期T1期、二次电切术后化疗药物灌注、泌尿系统肿瘤史和高PLR比值比是肿瘤复发的危险因素。综合分析以上4项临床指标，可有效评估NMIBC患者在接受二次电切术后的肿瘤复发风险，及时采取早期医疗干预措施以优化患者预后。

Abstract

Objective‍　‍To investigate risk factors for residual lesions after initial transurethral resection of bladder tumors (TURBT) and risk factors for tumor recurrence after second TURBT in patients with non-muscle-invasive bladder cancer (NMIBC) in order to provide reference for clinical management. Methods‍　‍A case-control study design was adopted to include 120 NMIBC patients who underwent initial TURBT and then second surgery within 2~8 weeks in our department from January 2017 to January 2025. Based on the presence of residual lesions after the initial TURBT or not

the patients were divided into a residual lesion group (

=34) and a non-residual lesion group (

=86).

Chi

-square test and multivariate logistic regression analysis were performed to identify potential risk factors for residual lesions following the initial TURBT. Univariate and multivariate Cox regression models were used to analyze potential risk factors for tumor recurrence after the second TURBT. Results‍　‍The residual lesion rate after initial TURBT was 28.33%.

Chi

-square test analysis revealed that tumor stage T1 (

Chi

-square=5.756

=0.016) and broad tumor base (

Chi

-square=4.331

=0.037) were factors influencing residual lesions after initial TURBT. Multivariate logistic regression analysis identified tumor stage T1 (

=3.047

95%

: 1.128~8.226

=0.028) as an independent risk factor for residual lesions after initial TURBT. The tumor recurrence rate after second TURBT was 17.5%. Multivariate Cox regression analysis identified tumor stage T1 (

=4.258

95%

: 1.248~14.5

=0.021)

intravesical chemotherapy instillation after second TURBT (

=3.539

95%

: 1.284~9.752

=0.015)

history of urinary system tumors (

=3.002

95%

: 1.145~7.873

=0.025) and high platelet-to-lymphocyte (PLR) ratio (

=2.798

95%

: 1.115~7.023

=0.028) as independent risk factors for tumor recurrence after second TURBT. Conclusion‍　‍Tumor stage T1 and broad tumor base are risk factors for residual lesions after initial TURBT

while tumor stage T1

intravesical chemotherapy instillation after second TURBT

history of urinary system tumors and high PLR ratio are risk factors for tumor recurrence after second TURBT. Comprehensive analysis on above 4 indicators can effectively assess the risk of tumor recurrence in NMIBC patients following second TURBT

and timely early medical intervention is beneficial for improving patient outcomes.

关键词

Keywords

references

FLAIG T W ， SPIESS P E ， AGARWAL N ， et al . Bladder cancer， version 3.2020， NCCN clinical practice guidelines in oncology ［J］. J Natl Compr Canc Netw ， 2020 ， 18 （ 3 ）： 329 - 354 . DOI： 10.6004/jnccn.2020.0011 http://dx.doi.org/10.6004/jnccn.2020.0011 .

DYRSKJØT L ， HANSEL D E ， EFSTATHIOU J A ， et al . Bladder cancer ［J］. Nat Rev Dis Primers ， 2023 ， 9 ： 58 . DOI： 10.1038/s41572-023-00468-9 http://dx.doi.org/10.1038/s41572-023-00468-9 .

OSMAN Y ， ELAWDY M ， TAHA D E ， et al . Bladder perforation as a complication of transurethral resection of bladder tumors： the predictors， management， and its impact in a series of 1570 at a tertiary urology institute ［J］. Int Urol Nephrol ， 2023 ， 55 （ 9 ）： 2161 - 2167 . DOI： 10.1007/s11255-023-03638-6 http://dx.doi.org/10.1007/s11255-023-03638-6 .

LIU S H ， FENG C C ， TAN L Y ， et al . Single-cell dissection of multifocal bladder cancer reveals malignant and immune cells variation between primary and recurrent tumor lesions ［J］. Commun Biol ， 2024 ， 7 （ 1 ）： 1659 . DOI： 10.1038/s42003-024-07343-7 http://dx.doi.org/10.1038/s42003-024-07343-7 .

BABJUK M ， BÖHLE A ， BURGER M ， et al . EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder： update 2016 ［J］. Eur Urol ， 2017 ， 71 （ 3 ）： 447 - 461 . DOI： 10.1016/j.eururo.2016.05.041 http://dx.doi.org/10.1016/j.eururo.2016.05.041 .

CHANG S S ， BOORJIAN S A ， CHOU R ， et al . Diagnosis and treatment of non-muscle invasive bladder cancer： AUA/SUO guideline ［J］. J Urol ， 2016 ， 196 （ 4 ）： 1021 - 1029 . DOI： 10.1016/j.juro.2016.06.049 http://dx.doi.org/10.1016/j.juro.2016.06.049 .

LICHTBROUN B ， SRIVASTAVA A ， GHODOUSSIPOUR S . A restaging transurethral resection of bladder tumor is always necessary for high-grade T1 non-muscle-invasive bladder cancer ［J］. Eur Urol Focus ， 2023 ， 9 （ 4 ）： 557 - 558 . DOI： 10.1016/j.euf.2023.05.010 http://dx.doi.org/10.1016/j.euf.2023.05.010 .

ISHII K ， YOKOYAMA Y ， NISHIDA Y ， et al . Characteristics of primary and repeated recurrent retroperitoneal liposarcoma： outcomes after aggressive surgeries at a single institution ［J］. Jpn J Clin Oncol ， 2020 ， 50 （ 12 ）： 1412 - 1418 . DOI： 10.1093/jjco/hyaa126 http://dx.doi.org/10.1093/jjco/hyaa126 .

GRAVESTOCK P ， COULTHARD N ， VEERATTERAPILLAY R ， et al . Systematic review and meta-analysis of narrow band imaging for non-muscle-invasive bladder cancer ［J］. Int J Urol ， 2021 ， 28 （ 12 ）： 1212 - 1217 . DOI： 10.1111/iju.14671 http://dx.doi.org/10.1111/iju.14671 .

中华医学会泌尿外科学分会，中国膀胱癌联盟 . 非肌层浸润性膀胱癌二次电切中国专家共识［J］. 中华泌尿外科杂志， 2017 ， 38 （ 8 ）： 561 - 563 . DOI： 10.3760/cma.j.issn.1000-6702.2017.08.001 http://dx.doi.org/10.3760/cma.j.issn.1000-6702.2017.08.001 .

Urology Branch of Chinese Medical Association， China Bladder Cancer Alliance . China expert consensus on secondary electroresection of non-muscular invasive bladder cancer ［J］. Chin J Urol ， 2017 ， 38 （ 8 ）： 561 - 563 . DOI： 10.3760/cma.j.issn.1000-6702.2017. 08.001 http://dx.doi.org/10.3760/cma.j.issn.1000-6702.2017.08.001 .

BABJUK M ， BURGER M ， CAPOUN O ， et al . European association of urology guidelines on non-muscle-invasive bladder cancer （Ta， T1， and carcinoma in situ）［J］. Eur Urol ， 2022 ， 81 （ 1 ）： 75 - 94 . DOI： 10.1016/j.eururo.2021. 08.010 http://dx.doi.org/10.1016/j.eururo.2021.08.010 .

Guigui A ， Basile G ， Zattoni F ， et al . Prognostic significance of residual tumor at restaging transurethral bladder resection in high-risk non-muscle-invasive bladder cancer ［J］. World J Urol ， 2024 ， 42 （ 1 ）： 480 . DOI： 10.1007/s00345-024-05192-x http://dx.doi.org/10.1007/s00345-024-05192-x .

CONTIERI R ， LUGHEZZANI G ， BUFFI N M ， et al . Could we safely avoid a second resection in selected patients with T1 non-muscle-invasive bladder cancer preliminary results of cost-effectiveness study from HUmanitas new indications for ReTUR （HuNIRe） multicenter prospective trial ［J］. Front Oncol ， 2022 ， 12 ： 879399 . DOI： 10.3389/fonc.2022.879399 http://dx.doi.org/10.3389/fonc.2022.879399 .

段利军 . 经尿道手术致尿道狭窄的原因分析及防治策略［J］. 现代医学与健康研究电子杂志， 2019 ， 3 （ 7 ）： 112 - 113 .

DUAN L J . Cause analysis and prevention strategy of urethral stricture caused by transurethral surgery ［J］. Mod Med Health Res ， 2019 ， 3 （ 7 ）： 112 - 113 .

DEL GIUDICE F ， VESTRI A ， FEGATELLI D A ， et al . VI-RADS followed by Photodynamic Transurethral Resection of Non-Muscle-Invasive Bladder Cancer vs White-Light Conventional and Second-resection： the ‘CUT-less’ Randomised Trial Protocol ［J］. BJU Int ， 2025 ， 135 （ 2 ）： 346 - 354 . DOI： 10.1111/bju.16531 http://dx.doi.org/10.1111/bju.16531 .

豆鹏，钟鑫，陈荣，等 . 高危非肌层浸润性膀胱癌首次电切术后肿瘤残余及二次电切术后复发相关危险因素分析［J］. 临床泌尿外科杂志， 2023 ， 38 （ 12 ）： 898 - 904， 909 . DOI： 10.13201/j.issn.1001-1420.2023.12.002 http://dx.doi.org/10.13201/j.issn.1001-1420.2023.12.002 .

DOU P ， ZHONG X ， CHEN R ， et al . Analysis of risk factors associated with tumor residue after first resection and recurrence after repeat transurethral resection for high risk non-muscle-invasive bladder cancer ［J］. J Clin Urol ， 2023 ， 38 （ 12 ）： 898 - 904， 909 . DOI： 10.13201/j.issn.1001-1420.2023.12.002 http://dx.doi.org/10.13201/j.issn.1001-1420.2023.12.002 .

DIAO M X ， LI Y ， GAO Z H ， et al . Comparison of prognosis after transurethral resection of bladder tumor between solitary and multiple bladder cancers ［J］. Medicine ， 2024 ， 103 （ 44 ）： e40314 . DOI： 10.1097/MD.0000000000040314 http://dx.doi.org/10.1097/MD.0000000000040314 .

KAWAI T ， MATSUYAMA H ， KOBAYASHI K ， et al . Photodynamic diagnosis-assisted transurethral resection of bladder tumor for high-risk non-muscle invasive bladder cancer improves intravesical recurrence-free survival （BRIGHT study）［J］. Int J Urol ， 2024 ， 31 （ 8 ）： 906 - 912 . DOI： 10.1111/iju.15483 http://dx.doi.org/10.1111/iju.15483 .

LIN L D ， GUO X T ， MA Y C ， et al . Does repeat transurethral resection of bladder tumor influence the diagnosis and prognosis of T1 bladder cancer A systematic review and meta-analysis ［J］. Eur J Surg Oncol ， 2023 ， 49 （ 1 ）： 29 - 38 . DOI： 10.1016/j.ejso.2022.06.005 http://dx.doi.org/10.1016/j.ejso.2022.06.005 .

NALLABOTHULA A K ， MUDUNURI H V V ， NALUMARU A S ， et al . Predicting the lymphovascular invasion in carcinoma bladder at transurethral resection ［J］. Cureus ， 2024 ， 16 （ 6 ）： e62595 . DOI： 10.7759/cureus.62595 http://dx.doi.org/10.7759/cureus.62595 .

程柏松，陈锦华，陈剑晖，等 . 非肌层浸润膀胱癌二次电切的临床意义及肿瘤复发的危险因素分析［J］. 福建医科大学学报， 2022 ， 56 （ 1 ）： 42 - 45 .

CHENG B S ， CHEN J H ， CHEN J H ， et al . The significance of repeated transurethral resection for non-muscle invasive bladder cancer and analysis of risk factors in recurrence of non-muscle invasive bladder cancer ［J］. J Fujian Med Univ ， 2022 ， 56 （ 1 ）： 42 - 45 .

REGNIER S ， CALIFANO G ， ELALOUF V ， et al . Restaging transurethral resection in ta high-grade nonmuscle invasive bladder cancer： a systematic review ［J］. Curr Opin Urol ， 2022 ， 32 （ 1 ）： 54 - 60 . DOI： 10.1097/MOU. 0000000000000949 http://dx.doi.org/10.1097/MOU.0000000000000949 .

JEONG S H ， HAN J H ， JEONG C W ， et al . Clinical determinants of recurrence in pTa bladder cancer following transurethral resection of bladder tumor ［J］. BMC Cancer ， 2022 ， 22 （ 1 ）： 631 . DOI： 10.1186/s12885-022-09733-8 http://dx.doi.org/10.1186/s12885-022-09733-8 .

陈伟，杨诚，梁朝朝 . 二次电切在非肌层浸润性膀胱肿瘤治疗中的意义及相关危险因素分析［J］. 安徽医科大学学报， 2018 ， 53 （ 12 ）： 1932 - 1937 . DOI： 10.19405/j.cnki.issn1000-1492.2018.12.025 http://dx.doi.org/10.19405/j.cnki.issn1000-1492.2018.12.025 .

CHEN W ， YANG C ， LIANG C Z . Significance of repeated transurethral resection of bladder tumor and analysis of related risk factors ［J］. Acta Univ Med Anhui ， 2018 ， 53 （ 12 ）： 1932 - 1937 . DOI： 10.19405/j.cnki.issn1000-1492.2018.12.025 http://dx.doi.org/10.19405/j.cnki.issn1000-1492.2018.12.025 .

JANJI B ， CHOUAIB S . The promise of targeting hypoxia to improve cancer immunotherapy： mirage or reality ［J］. Front Immunol ， 2022 ， 13 ： 880810 . DOI： 10.3389/fimmu. 2022.880810 http://dx.doi.org/10.3389/fimmu.2022.880810 .

MALMSTRÖM P U ， SYLVESTER R J ， CRAWFORD D E ， et al . An individual patient data meta-analysis of the long-term outcome of randomised studies comparing intravesical mitomycin C versus Bacillus Calmette-Guérin for non-muscle-invasive bladder cancer ［J］. Eur Urol ， 2009 ， 56 （ 2 ）： 247 - 256 . DOI： 10.1016/j.eururo.2009.04.038 http://dx.doi.org/10.1016/j.eururo.2009.04.038 .

LIATSOS G D ， MARIOLIS I ， HADZIYANNIS E ， et al . Review of BCG immunotherapy for bladder cancer ［J］. Clin Microbiol Rev ， 2025 ， 38 （ 1 ）： e0019423 . DOI： 10.1128/cmr.00194-23 http://dx.doi.org/10.1128/cmr.00194-23 .

ANTONELLI A C ， BINYAMIN A ， HOHL T M ， et al . Bacterial immunotherapy for cancer induces CD4-dependent tumor-specific immunity through tumor-intrinsic interferon-γ signaling ［J］. Proc Natl Acad Sci USA ， 2020 ， 117 （ 31 ）： 18627 - 18637 . DOI： 10.1073/pnas.2004421117 http://dx.doi.org/10.1073/pnas.2004421117 .

Massari M ， O'Malley P ， Benidir T ， et al . Efficacy of BCG for non-muscle invasive bladder cancer following nephroureterectomy for upper tract urothelial carcinoma ［J］. Urol Oncol ， 2024 ， 42 （ 9 ）： 287 - 289 . DOI： 10.1016/j.urolonc.2024.05.007 http://dx.doi.org/10.1016/j.urolonc.2024.05.007

DING L ， DENG X B ， WANG K ， et al . Preoperative systemic inflammatory markers as a significant prognostic factor after TURBT in patients with non-muscle-invasive bladder cancer ［J］. J Inflamm Res ， 2023 ， 16 ： 283 - 296 . DOI： 10.2147/JIR.S393511 http://dx.doi.org/10.2147/JIR.S393511 .

ZHU T Y ， CHEN Z Y ， ZHANG B C ， et al . Prognostic value of platelet to lymphocyte ratio in patients with cervical cancer： an updated systematic review and meta-analysis ［J］. World J Surg Oncol ， 2025 ， 23 （ 1 ）： 187 . DOI： 10.1186/s12957-025-03838-7 http://dx.doi.org/10.1186/s12957-025-03838-7 .

董超男，翟文萍，王雪野 . 血小板介导肿瘤细胞生长和转移的机制研究进展［J］. 医学综述， 2020 ， 26 （ 4 ）： 695 - 699 . DOI： 10.3969/j.issn.1006-2084.2020.04.014 http://dx.doi.org/10.3969/j.issn.1006-2084.2020.04.014 .

DONG C N ， ZHAI W P ， WANG X Y . Research progress in mechanism of platelet-mediated tumor cell growth and metastasis ［J］. Med Recapitul ， 2020 ， 26 （ 4 ）： 695 - 699 . DOI： 10.3969/j.issn.1006-2084.2020.04.014 http://dx.doi.org/10.3969/j.issn.1006-2084.2020.04.014 .

TALMAC M A ， CIFTPINAR T ， OZDEMIR M S ， et al . Can the combination of magnetic resonance imaging， neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio predict the mass origin in ovarian masses ［J］. Sisli Etfal Hastan Tı ；p Bul， 2023 ， 57 （ 3 ）： 326 - 331 . DOI： 10.14744/SEMB.2023.47529 http://dx.doi.org/10.14744/SEMB.2023.47529 .

WU H M ， WANG Y Z ， DENG M ， et al . Preoperative inflammatory markers and tumor markers in predicting lymphatic metastasis and postoperative complications in colorectal cancer： a retrospective study ［J］. BMC Surg ， 2025 ， 25 （ 1 ）： 71 . DOI： 10.1186/s12893-025-02795-y http://dx.doi.org/10.1186/s12893-025-02795-y .

王海涛，罗伟铭，陈剑，等 . 中高危非肌层浸润性膀胱癌卡介苗灌注治疗后复发的临床预测模型构建与验证［J］. 陆军军医大学学报， 2025 ， 47 （ 9 ）： 959 - 968 . DOI： 10.16016/j.2097-0927.202501061 http://dx.doi.org/10.16016/j.2097-0927.202501061 .

WANG H T ， LUO W M ， CHEN J ， et al . Development and validation of clinical prediction model for post-treatment recurrence in high-risk non-muscle invasive bladder cancer after BCG intravesical instillation ［J］. J Army Med Univ ， 2025 ， 47 （ 9 ）： 959 - 968 . DOI： 10.16016/j.2097-0927.202501061 http://dx.doi.org/10.16016/j.2097-0927.202501061 .

Views

下载量

CSCD

Alert me when the article has been cited

提交

Tools

Publicity Resources

Incidence and risk factors of acute renal injury after Stanford type A aortic dissections

Predictive value and risk factors of embryo implantation site for placenta previa

Construction and validation of a risk prediction model for lean metabolic dysfunction-associated steatotic liver disease

Risk factors for hospitalization within 24 h postnatally and respiratory support in late preterm and term neonates

Progress and prospective of environmental, lifestyle and psychological risk factors for reproductive impairment and adverse birth outcome

Related Author

XU Xiao

LI Xiaodong

WEN Jing

NING Jiaolin

KUANG Na

HE Wenjiao

XIONG Xi

CHEN Zhengqiong

Related Institution

Department of Anesthesiology， First Affiliated Hospital， Army Medical University （Third Military Medical University）

Department of Obstetrics and Gynecology， Second Affiliated Hospital， Army Medical University （Third Military Medical University）

Department of Gastroenterology， First Affiliated Hospital， Army Medical University（Third Military Medical University）

Department of Pediatrics，University-Town Hospital of Chongqing Medical University

Department of Pediatrics，the Second Affiliated Hospital of Chongqing Medical University

⁰